RESEARCH ARTICLE

Factors Associated With Readmission in Late-Preterm Infants: A Matched Case-Control Study abstract OBJECTIVE: The goal of this study was to evaluate risk factors for readmission among late-preterm (34–36 weeks’ gestation) infants in clinical practice. METHODS: This was a retrospective, matched case-control study of latepreterm infants receiving care across 8 regional hospitals in 2009 in the United States. Those readmitted within 28 days of birth were matched to non-readmitted infants at a ratio of 1:3 according to birth hospital, birth month, and gestational age. Step-wise modeling with likelihood ratio tests were used to develop a multivariable logistic regression model. A subgroup analysis of hyperbilirubinemia readmissions was also performed. RESULTS: Of 1861 late-preterm infants delivered during the study period, 67 (3.6%) were readmitted within 28 days of birth. These were matched to 201 control infants, for a final sample of 268 infants. In multivariable regression, each additional day in length of stay was associated with a significantly reduced odds ratio (OR) for readmission (0.57, P = .004); however, for those infants delivered vaginally, there was no significant association between length of stay and readmission (adjusted OR: 1.08, P = .16). A stronger inverse relationship was observed in subgroup analysis for hyperbilirubinemia readmissions, with the adjusted OR associated with increased length of stay 0.40 (P = .002) for infants born by cesarean delivery but 1.14 (P = .27) for those delivered vaginally. CONCLUSIONS: Infants born via cesarean delivery with longer length of hospital stay have a decreased risk for readmission. As hospitals implement protocols to standardize length of stay, mode of delivery may be a useful factor to identify late-preterm infants at higher risk for readmission.

AUTHORS Laurel B. Moyer, MD, MPH,1 Neera K. Goyal, MD, Msc,1,2 Jareen Meinzen-Derr, PhD, MPH, 3 Laura P. Ward, MD,1 Christina L. Rust, MSN,4 Scott L. Wexelblatt, MD,1 and James M. Greenberg, MD1 1

Divisions of Neonatology and Perinatal Institute, Hospital Medicine, Cincinnati Children’s Research Foundation and Department of Pediatrics, 3 Division of Biostatistics and Epidemiology, Cincinnati Children’s Hospital Medical Center, University of Cincinnati College of Medicine, Cincinnati, Ohio; and 4 Department of Obstetrics, St. Elizabeth’s Healthcare 2

KEY WORDS cesarean delivery, delivery, hyperbilirubinemia, late preterm, length of stay, readmission ABBREVIATIONS CI: confidence interval OR: odds ratio All authors participated in the concept and design, analysis and interpretation of data, and drafting or revising of the manuscript. All authors approved the manuscript as submitted. Address correspondence to Laurel B. Moyer, MD, MPH, Cincinnati Children’s Hospital Medical Center, Division of Neonatology, MLC 7009, 3333 Burnet Ave, Cincinnati, OH 45229-3039. E-mail: [email protected] www.hospitalpediatrics.org doi:10.1542/hpeds.2013-0120 HOSPITAL PEDIATRICS (ISSN Numbers: Print, 2154 - 1663; Online, 2154 - 1671).

Late-preterm infants, defined as infants born at 34 to 36 weeks’ gestation,1 have an increased risk of morbidity and complications compared with term infants (born at ≥37 weeks’ gestation).2–7 Previous studies demonstrated that late-preterm infants may be up to 3 times more likely to be readmitted than term infants,5,8,9 most commonly for hyperbilirubinemia, sepsis evaluation, and feeding difficulties,1,2,10–13 with the overall readmission rate progressively increasing as gestational age decreases from 40 weeks.14 It is estimated that >250 000 late-preterm births occur in the United States each year.15 Given this contribution to neonatal hospitalizations and health care spending, as well as the significant variability in late-preterm readmissions attributed to lack of standardized care,11,16 reduction of hospital readmission for this population represents an important area for potential improvements in hospital care quality.

Copyright © 2014 by the American Academy of Pediatrics FINANCIAL DISCLOSURE: The authors have indicated they have no financial relationships relevant to this article to disclose. FUNDING: No external funding. POTENTIAL CONFLICT OF INTEREST: The authors have indicated they have no potential conflicts of interest to disclose.

Infant factors associated with increased readmission risk among late-preterm infants are well described and include being the first-born child, male gender, maternal 298 |

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delivery complications, initial discharge from the normal newborn nursery rather than an ICU, breastfeeding, Asian/Pacific Island descent, and public insurance status.6,9,12,14 However, there is limited evidence to support models of discharge care that effectively mitigate this outcome.17 In fact, some evidence suggests that over time, readmission rates have increased for this population.18 One challenge to developing a standardized approach to discharge may be difficulty in appropriately identifying infants at highest risk for readmission in real time, before discharge. With birth weights often comparable to term infants, many late-preterm infants receive routine newborn hospital care postpartum and may not present with feeding inadequacy or other complications until after discharge. However, previous studies of both late-preterm and term infants have failed to demonstrate that longer length of stay actually reduces readmission risk.9,18–21 In addition, given that the most common indication for neonatal readmission, hyperbilirubinemia, generally develops after the first 2 days of life, any benefit from delaying hospital discharge on readmission risk may be differentially observed for this diagnosis compared with other indications for readmission. The present study takes advantage of access to a regionally defined, populationbased cohort of late-preterm readmitted and non-readmitted infants. Our objective was to evaluate risk factors for neonatal readmission, adjusting for variation in care across multiple hospitals, with the goal of informing more effective approaches for risk stratification in clinical practice.

METHODS

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newborn service across 8 hospitals provided by the Cincinnati Children’s Hospital Medical Center Division of Neonatology. Providers serve all newborn infants requiring intensive care in greater Cincinnati and ∼85% of all healthy infants born in the region. With >30 000 annual regional births, distributed across high- and low-volume academic and community hospitals, this service is one of the largest and most comprehensive programs of care for newborns in the United States managed by a single academic clinician group. Of the 8 hospitals included in our study, 5 incorporate Level I and II nurseries, 2 have Level I and IIIB nurseries, and 1 freestanding children’s hospital has a Level IIIC NICU. The target population was late-preterm infants born January 1, 2009, to December 31, 2009, and admitted to 1 of these 8 area hospitals. All infants who met condition eligibility criteria (gestational age 34 0/7 through 36 6/7 weeks) were included for potential selection into the study sample. At the time this study was conducted, no institutional policy for late-preterm infant care had been implemented. Discharge decisions regarding length of stay, attained weight, or feeding criteria were at the treating physician’s discretion, and policies regarding criteria for Level II or Level III nursery admission varied according to each hospital. Institutional human subjects review board approval was obtained from all participating study hospitals. The study was determined to pose minimal risk to the participants as a retrospective chart review.

Setting and Study Population

Data Sources and Study Design

The setting for this study was a regional, population-based clinical

Data for this retrospective, matched case-control study were derived from

maternal and infant birth hospitalization records as well as readmission records. First, all late-preterm infants readmitted within 28 days of birth (case subjects) were identified through manual chart review for each study hospital. A control population of non-readmitted late-preterm infants for each hospital was then chosen by using birth certificate data provided by the Ohio Department of Health. Cases were then matched to a sample of control infants who were not readmitted within 28 days. For each case infant, a pool of control infants matched on birth hospital and gestational age was defined. To account for seasonal variation in readmissions, control infants were also matched to case subjects based on month of birth. From this matched pool of controls, 3 control infants were selected for each case infant by using random number sequencing. In the situation in which there were not 3 control births in the relevant month, the month before or after was used. Analytic Variables and Outcomes

For both case and control subjects, data were abstracted from maternal and infant hospital records. Variables were selected a priori based on their availability in the data sources and their potential relevance for readmission: birth hospital, maternal age, race, type of insurance, marital status, parity, infant gestational age at time of delivery, mode of delivery, pregnancy and delivery complications, maternal and infant blood type, infant gender, birth and discharge weight, Apgar scores, feeding method, performance of bilirubin screening, and length of hospital stay. Because bilirubin screening was not performed for all infants, and because in many cases the

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transcutaneous bilirubin level was not documented in the medical record, we only assessed whether any screening was performed. For those readmitted infants, age and weight at readmission were also obtained. Indications for readmission were ascertained based on chart review and grouped into categories similar to those in previous studies (ie, hyperbilirubinemia, feeding difficulties, hypothermia, sepsis evaluation).11,22 Categories were not mutually exclusive, such that >1 category were assigned to some infants.

Sample size determinations were based on the probability of exposure in the control subjects, assuming a fixed α level of 0.05, power of 80%, and an estimated correlation coefficient for exposures between case and control subjects of 0.2.23 First, data distributions were assessed by using means ± SDs and/or medians with ranges and interquartile ranges, frequencies, and proportions. Bivariate analyses were then conducted by using unadjusted (simple) conditional logistic regression, which tested for differences between the matched case and control subjects. Step-wise modeling with covariates deemed to be empirically or statistically important (P < .20) was used to develop a parsimonious multivariable conditional logistic regression model. Due to large observed differences in readmission according to mode of delivery, we made a decision to test the effect of an interaction term between mode of delivery and length of stay in the model; this finding was statistically significant (P < .05) and was retained in the final model. Finally, we conducted a subgroup analysis of control and case infants readmitted for hyperbilirubinemia VOLUME 4 • ISSUE 5

All statistical tests were 2-sided, and statistical significance was defined as P < .05. Analyses were performed by using SAS version 9.3 (SAS Institute, Inc, Cary, NC).

RESULTS

Data Analysis

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only, as this diagnosis was associated with a shorter mean length of stay and younger mean age at readmission compared with other readmission diagnoses. The Akaike information criterion and –2 log-likelihood values were used to help assess the fitness of the model.

Of 1861 late-preterm infants delivered at 8 hospitals during the study period, 67 were readmitted within 28 days of birth, resulting in a late-preterm readmission rate of 3.6%. The percentage of infants readmitted varied 3.5-fold between hospitals, ranging from 2.0% to 6.9%. The majority of readmissions (75%) occurred due to hyperbilirubinemia, with 34% of readmissions categorized as relating to feeding problems, 12% as hypothermia, and 4% as suspected infection. The average age at readmission was 7.3 days; however, age varied according to infant’s readmission diagnosis. The mean age at readmission was the youngest (4.5 days) for those infants with hyperbilirubinemia, whereas the mean age at readmission for feeding problems, hypothermia, and suspected infection was 10.4, 9.3, and 13.0 days, respectively (Table 1). Matching all 67 readmitted infants to control infants at a ratio of 1:3 resulted

in a final analytic sample size of 268 late-preterm infants. Bivariate Analysis

There were no statistical differences between the case and control groups regarding birth weight, gender, or singleton versus multiple birth (Table 2). Bivariate comparisons demonstrated a statistically significant association between mode of delivery and readmission status, with readmitted infants more likely to be delivered vaginally compared with non-readmitted infants (75% vs 55%; P = .003). In bivariate analyses, feeding method also differed significantly according to readmission status, with 49% of non-readmitted infants versus 34% of readmitted infants receiving formula exclusively (P = .03). Other significant differences according to readmission status included mean length of stay (P = .04) and performance of screening bilirubin (P = .009) before nursery discharge. In both groups, most mothers received prenatal care, were non-Hispanic white, multiparous, and had private insurance. There was no statistical difference between case and control subjects in maternal parity, admission status after delivery (NICU versus normal newborn nursery), or discharge weight. Multivariate Analysis for all Readmissions

As stated earlier, an interaction term between delivery mode and length of stay was tested and was statistically

TABLE 1 Length of Stay and Timing of Readmission by Diagnostic Category (N = 67) Indication for Readmission

Age at Initial Discharge

Age at Readmission

Hyperbilirubinemia, n = 50 Feeding difficulty, n = 23 Hypothermia, n = 8 Suspected infection, n = 16

2.4 ± 1.3 5.5 ± 5.2 6.3 ± 6.3 5.3 ± 4.3

4.5 ± 2.2 10.4 ± 8.1 9.3 ± 7.3 13.0 ± 7.4

Data are presented as mean ± SD in days. Diagnostic categories are not mutually exclusive.

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TABLE 2 Unadjusted Clinical and Demographic Characteristics of Infants Readmitted Versus Not Readmitted (N = 268) Characteristic

Readmitted (n = 67)

Mode of delivery, % (n) Cesarean Vaginal Length of stay, d Mean ± SD Median (range) Admission status, % (n) Newborn nursery NICU/special care nursery Feeding method, % (n) Exclusive breastfeeding Exclusive bottle-feeding Both breastfeeding and bottle-feeding Bilirubin screening before discharge Gender, % (n) Male Female Birth weight, mean ± SD, g Singleton pregnancy, % (n) Singleton Multiple Maternal age, mean ± SD, y Gravidity, mean ± SD Primiparous status Race, % (n) Non-Hispanic white Black Other Unknown Ethnicity, % (n) Non-Hispanic Hispanic Unknown Insurance type, % (n) Private insurance Public insurance/self-pay

25.4 (17) 74.6 (50) 3.7 + 3.6 2.5 (1–20)

Not Readmitted (n = 201) 45.3 (91) 54.7 (110) 4.6 + 4.8 3.0 (0.5–37)

a OR

95% CIa

P

0.38 Ref

0.20–0.72 —

.003 —

0.6b —

0.38–0.98 —

.04b —

64.2 (43) 38.8 (26)

64.7 (130) 37.3 (75)

0.97 1.09

0.50–1.90 0.56–2.15

.93 .79

31.3 (21) 34.3 (23) 34.3 (23) 74.6 (50)

27.4 (55) 48.8 (98) 23.9 (48) 115 (57.2)

— 0.52c — 2.44

— 0.29–0.96 — 1.25–4.73

— .03c — .009

59.7 (40) 40.2 (27) 2703 ± 559

47.8 (96) 52.2 (105) 2584 ± 472

1.65 Ref 1.001

0.93–2.92 — 1.00, 1.001

.09 — .06

79.1 (53) 20.9 (14) 28.2 ± 6.1 2.36 ± 1.8 37.3 (25)

84.1 (169) 15.9 (32) 27.9 + 6.3 2.39 ± 1.4 35.3 (71)

0.68 Ref — 0.99 1.09

0.32–1.46 — — 0.82–1.19 0.61–1.96

.32 — .70 .90 .80

82.0 (55) 12.0 (8) 4.5 (3) 1.5 (1)

82.1 (165) 13.4 (27) 3.0 (6) 1.5 (3)

1.0d — — —

0.46–2.17 — — —

.42d — — —

91.0 (61) 7.5 (5) 1.5 (1)

79.1 (159) 3.5 (7) 17.4 (35)

1.62 Ref —

0.47–5.58 — —

.44 — —

65.7 (44) 34.3 (23)

61.2 (123) 38.8 (78)

1.22 Ref

0.68–2.20 —

.51 —

—, not applicable. a

ORs and 95% CIs derived from simple conditional logistic regression, accounting for matching characteristics of gestational age, birth hospital, and month of birth. P value for comparison of log-transformed values. c P value for comparison of any breastfeeding with exclusive bottle-feeding. d P value for comparison of white versus non-white. b

significant. Among vaginally delivered infants, the mean length of stay was 3.5 days, with a median of 2 days and a range of 1 to 37 days. Among those born via cesarean delivery, mean length of stay was 5.8 days, with a median of 3.5 days and a range of 0.5 to 26 days. The multivariable conditional logistic regression model derived through stepwise modeling is shown in Table 3 and included birth

weight, bilirubin screening before discharge, admission to a NICU/special care nursery, and the interaction term between delivery mode and length of stay. Adjusting for all covariates, each additional day in length of stay was associated with a significantly reduced odds ratio (OR) for readmission (0.57 [95% confidence interval (CI): 0.39–0.84]); however, this association was only observed for infants

born by cesarean delivery. For those delivered vaginally, there was no significant association between length of stay and readmission (adjusted OR: 1.08 [95% CI: 0.97–1.20]). Subanalysis for Hyperbilirubinemia

Based on differences in length of stay and age at readmission for infants admitted for hyperbilirubinemia, a subgroup analysis was performed for 46

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TABLE 3 Multivariable Conditional Logistic Regression Model for All Readmissions Within 28 Days, aOR, and 95% CIs (N = 268) Variable a

Infant birth weight, g Discharge bilirubin data available Level II or III nursery care Age at discharge by mode of deliveryb Discharge age for vaginal delivery Discharge age for cesarean delivery

aOR

95% CI

P

1.07 3.39 2.52 — 1.08 0.57

0.995–1.16 1.64–7.00 1.03–6.17 — 0.97–1.20 0.39–0.84

.07 .001 .04 .001 .16 .004

Study design adjusts for matching characteristics of gestational age, birth hospital, and month of birth. a Coefficient represents adjusted OR (aOR) for every increase in 100 g. b Interaction between age at discharge and delivery. Coefficient represents aOR for each additional day in length of stay.

case infants with hyperbilirubinemia and their matched 138 control subjects. Four additional infants admitted for both infection and hyperbilirubinemia were omitted from this analysis. The multivariable conditional logistic regression model derived through stepwise modeling for this subgroup is shown in Table 4 and included birth weight, feeding method, bilirubin screening before discharge, and the interaction term between delivery mode and length of stay. As with the multivariable analysis results for the full sample, an association between increased length of stay and adjusted OR of readmission was only observed for infants born by cesarean delivery (adjusted OR: 0.40 [95% CI: 0.22– 0.72]). For those delivered vaginally, there was no significant association between increasing length of stay and readmission (adjusted OR: 1.14 [95% CI: 0.90–1.45]).

DISCUSSION Readmissions during the neonatal period account for >100 000 hospitalizations each year,24 and they are increasingly recognized as an outcome of importance to families, hospital, and payers. Late-preterm infants represent a population that is particularly at risk; in fact, recent evidence suggests that in the immediate weeks after discharge, they are perhaps even more vulnerable than infants born at earlier gestational ages due to a combination of immature physiology and lower intensity of hospital and followup services.22 Despite extensive previous literature demonstrating the increased risk of late-preterm infants for readmission, there remains limited evidence to guide the development of hospital-based approaches to discharge management for this population.2 Length of stay in particular has been evaluated for its potential effect

TABLE 4 Multivariable Conditional Logistic Regression Model for Hyperbilirubinemia Readmissions, aOR, and 95% CIs (N = 46) Variable a

Infant birth weight, g Bottle-fed only Discharge bilirubin data available Age at discharge by mode of deliveryb Discharge age for vaginal delivery Discharge age for cesarean delivery

aOR

95% CI

P

1.19 0.27 8.76 — 1.14 0.40

1.02–1.40 0.08–0.86 2.54–30.25 — 0.90–1.45 0.22–0.72

.03 .03

Factors associated with readmission in late-preterm infants: a matched case-control study.

The goal of this study was to evaluate risk factors for readmission among late-preterm (34-36 weeks' gestation) infants in clinical practice...
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